Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Selective molecular transport through the protein shell of a bacterial microcompartment organelle

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [2];  [3];  [3];  [1];  [4];  [1]
  1. Iowa State Univ., Ames, IA (United States). Roy J. Carver Dept. of Biochemistry, Biophysics, and Molecular Biology
  2. Univ. of California, Los Angeles, CA (United States). Molecular Biology Inst.
  3. Univ. of California, Los Angeles, CA (United States). UCLA-DOE Inst. for Genomics and Proteomics
  4. Univ. of California, Los Angeles, CA (United States). Molecular Biology Inst. UCLA-DOE Inst. for Genomics and Proteomics. Dept. of Chemistry and Biochemistry
Bacterial microcompartments are widespread prokaryotic organelles that have important and diverse roles ranging from carbon fixation to enteric pathogenesis. Current models for microcompartment function propose that their outer protein shell is selectively permeable to small molecules, but whether a protein shell can mediate selective permeability and how this occurs are unresolved questions. In this paper, biochemical and physiological studies of structure-guided mutants are used to show that the hexameric PduA shell protein of the 1,2-propanediol utilization (Pdu) microcompartment forms a selectively permeable pore tailored for the influx of 1,2-propanediol (the substrate of the Pdu microcompartment) while restricting the efflux of propionaldehyde, a toxic intermediate of 1,2-propanediol catabolism. Crystal structures of various PduA mutants provide a foundation for interpreting the observed biochemical and phenotypic data in terms of molecular diffusion across the shell. Finally and overall, these studies provide a basis for understanding a class of selectively permeable channels formed by nonmembrane proteins.
Research Organization:
Iowa State Univ., Ames, IA (United States); Univ. of California, Los Angeles, CA (United States)
Sponsoring Organization:
National Inst. of Health (NIH) (United States); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Grant/Contract Number:
AC02-06CH11357
OSTI ID:
1172992
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 10 Vol. 112; ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)Copyright Statement
Country of Publication:
United States
Language:
ENGLISH

References (37)

Bacterial microcompartments: their properties and paradoxes journal November 2008
Insights from multiple structures of the shell proteins from the β-carboxysome journal January 2008
Using comparative genomics to uncover new kinds of protein-based metabolic organelles in bacteria: Bacterial Microcompartments journal January 2013
Radical catalysis of B12 enzymes: structure, mechanism, inactivation, and reactivation of diol and glycerol dehydratases journal January 2000
PduP is a coenzyme-a-acylating propionaldehyde dehydrogenase associated with the polyhedral bodies involved in B 12 -dependent 1,2-propanediol degradation by Salmonella enterica serovar Typhimurium LT2 journal November 2003
Polyhedral organelles compartmenting bacterial metabolic processes journal March 2006
Identification and Structural Analysis of a Novel Carboxysome Shell Protein with Implications for Metabolite Transport journal September 2009
Alanine Scanning Mutagenesis Identifies an Asparagine–Arginine–Lysine Triad Essential to Assembly of the Shell of the Pdu Microcompartment journal June 2014
The protein shells of bacterial microcompartment organelles journal April 2011
Engineering Bacterial Microcompartment Shells: Chimeric Shell Proteins and Chimeric Carboxysome Shells journal July 2014
Solvation energy in protein folding and binding journal January 1986
Protein-based organelles in bacteria: carboxysomes and related microcompartments journal August 2008
Ethanolamine utilization in bacterial pathogens: roles and regulation journal April 2010
Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota journal October 2011
Structural Insight into the Mechanisms of Transport across the Salmonella enterica Pdu Microcompartment Shell journal September 2010
Protein Structures Forming the Shell of Primitive Bacterial Organelles journal August 2005
Atomic-Level Models of the Bacterial Carboxysome Shell journal February 2008
Structure and Mechanisms of a Protein-Based Organelle in Escherichia coli journal December 2009
The Structure of the Potassium Channel: Molecular Basis of K+ Conduction and Selectivity journal April 1998
Utilization of Glycerol as a Hydrogen Acceptor by Lactobacillus reuteri: Purification of 1,3-Propanediol:NAD+ Oxidoreductase † journal January 1990
Crystallographic Insights into the Pore Structures and Mechanisms of the EutL and EutM Shell Proteins of the Ethanolamine-Utilizing Microcompartment of Escherichia coli journal September 2010
Genetic Analysis of the Protein Shell of the Microcompartments Involved in Coenzyme B12-Dependent 1,2-Propanediol Degradation by Salmonella journal January 2011
Lactobacillus reuteri DSM 20016 Produces Cobalamin-Dependent Diol Dehydratase in Metabolosomes and Metabolizes 1,2-Propanediol by Disproportionation journal May 2008
Microcompartments for B12-Dependent 1,2-Propanediol Degradation Provide Protection from DNA and Cellular Damage by a Reactive Metabolic Intermediate journal February 2008
Evidence that a Metabolic Microcompartment Contains and Recycles Private Cofactor Pools journal April 2013
The PduM Protein Is a Structural Component of the Microcompartments Involved in Coenzyme B12-Dependent 1,2-Propanediol Degradation by Salmonella enterica journal February 2012
The Propanediol Utilization (pdu) Operon ofSalmonella enterica Serovar Typhimurium LT2 Includes Genes Necessary for Formation of Polyhedral Organelles Involved in Coenzyme B12-Dependent 1,2-Propanediol Degradation † journal January 1999
PduA Is a Shell Protein of Polyhedral Organelles Involved in Coenzyme B12-Dependent Degradation of 1,2-Propanediol in Salmonella enterica Serovar Typhimurium LT2 journal March 2002
Protein Content of Polyhedral Organelles Involved in Coenzyme B12-Dependent Degradation of 1,2-Propanediol in Salmonella enterica Serovar Typhimurium LT2 journal August 2003
Minimal Functions and Physiological Conditions Required for Growth of Salmonella enterica on Ethanolamine in the Absence of the Metabolosome journal November 2005
Conserving a Volatile Metabolite: a Role for Carboxysome-Like Organelles in Salmonella enterica journal April 2006
Diverse Bacterial Microcompartment Organelles journal September 2014
Functions, Compositions, and Evolution of the Two Types of Carboxysomes: Polyhedral Microcompartments That Facilitate CO2 Fixation in Cyanobacteria and Some Proteobacteria journal September 2013
Utilization of Glycerol as a Hydrogen Acceptor by Lactobacillus reuteri: Purification of 1,3-Propanediol:NAD+ Oxidoreductase † journal January 1990
Bacterial Microcompartments journal January 2007
Bacterial Microcompartments journal October 2010
The Shells of BMC-Type Microcompartment Organelles in Bacteria journal January 2013

Cited By (29)

Encapsulation mechanisms and structural studies of GRM2 bacterial microcompartment particles journal January 2020
Engineering formation of multiple recombinant Eut protein nanocompartments in E. coli journal April 2016
Effect of bio-engineering on size, shape, composition and rigidity of bacterial microcompartments journal November 2016
Coenzyme B12 synthesis as a baseline to study metabolite contribution of animal microbiota journal June 2017
Transfer and analysis of Salmonella pdu genes in a range of Gram-negative bacteria demonstrate exogenous microcompartment expression across a variety of species journal October 2017
Bacterial microcompartments: catalysis-enhancing metabolic modules for next generation metabolic and biomedical engineering journal October 2019
Development of an efficient technique for gene deletion and allelic exchange in Geobacillus spp. journal April 2017
All-atom normal mode dynamics of HIV-1 capsid journal September 2018
Apparent size and morphology of bacterial microcompartments varies with technique journal March 2020
Engineering bacterial microcompartments with heterologous enzyme cargos journal September 2016
Encapsulation of multiple cargo proteins within recombinant Eut nanocompartments journal July 2016
The Phenix software for automated determination of macromolecular structures journal September 2011
HIV-1 uses dynamic capsid pores to import nucleotides and fuel encapsidated DNA synthesis journal August 2016
Engineered synthetic scaffolds for organizing proteins within the bacterial cytoplasm journal December 2017
Enzymatic reactions in confined environments journal May 2016
Bacterial microcompartments journal March 2018
Control of enzyme reactions by a reconfigurable DNA nanovault journal October 2017
Functional protein shells fabricated from the self-assembling protein sheets of prokaryotic organelles journal January 2020
Bio-engineering of bacterial microcompartments: a mini review journal June 2019
Localization of Proteins to the 1,2-Propanediol Utilization Microcompartment by Non-native Signal Sequences Is Mediated by a Common Hydrophobic Motif journal August 2015
Proteomic Delineation of the ArcA Regulon in Salmonella Typhimurium During Anaerobiosis journal July 2018
Fast normal mode computations of capsid dynamics inspired by resonance journal April 2018
Engineering the PduT shell protein to modify the permeability of the 1,2-propanediol microcompartment of Salmonella journal December 2019
Bacterial microcompartments: widespread prokaryotic organelles for isolation and optimization of metabolic pathways: Bacterial microcompartments journal August 2015
The function of the PduJ microcompartment shell protein is determined by the genomic position of its encoding gene: Function of the PduJ microcompartment shell protein journal June 2016
A Bacterial Microcompartment Is Used for Choline Fermentation by Escherichia coli 536 journal March 2018
The N Terminus of the PduB Protein Binds the Protein Shell of the Pdu Microcompartment to Its Enzymatic Core journal January 2017
Bacterial Microcompartments journal January 2007
Bacterial Microcompartments journal October 2010

Similar Records

Alanine Scanning Mutagenesis Identifies an Asparagine–Arginine–Lysine Triad Essential to Assembly of the Shell of the Pdu Microcompartment
Journal Article · Sun Jun 01 00:00:00 EDT 2014 · Journal of Molecular Biology · OSTI ID:1132645

The function of the PduJ microcompartment shell protein is determined by the genomic position of its encoding gene
Journal Article · Mon Jun 06 20:00:00 EDT 2016 · Molecular Microbiology · OSTI ID:1328044

Self-assembling Shell Proteins PduA and PduJ have Essential and Redundant Roles in Bacterial Microcompartment Assembly
Journal Article · Fri Nov 20 19:00:00 EST 2020 · Journal of Molecular Biology · OSTI ID:1853101